John, who was a younger son, acquired his landed holdings for the most part through purchase and marriage. One such purchase was the manor of Denham and lands in Eye (Suffolk), which he acquired before 1381 but relinquished in 1402. His first marriage, to a member of the family of Zouche, brought him South Charford in the Avon valley in Hampshire as well as Eynesbury and other properties in Huntingdonshire. Under the terms of the agreement made in preparation for his second marriage, Popham’s future father-in-law, Sir Walter Romsey, promised to entail the large manor of Rockbourne on him and his future wife and their issue, and in November 1400, after the wedding had taken place, Popham procured the necessary royal licence for the settlement. But Sir Walter then refused to carry out his promise and, indeed, two years later entailed Rockbourne in favour of his grandson, Thomas Romsey. Amicable relations with the Romseys were resumed later, but Popham never acquired Rockbourne. His second wife did, however, bring him possession, for her lifetime, of her dower from a previous husband, which included the manor and advowson of Staunton Fitzherberd near Highworth in Wiltshire. Popham also held substantial properties in Salisbury and Southampton, the latter dating from his time as constable of Southampton castle. According to the assessments made in 1412 his lands in Hampshire were worth £20 a year, those in Huntingdonshire £31 and those in Wiltshire 19 marks, making a total of £63 13s.4d.
Although he is first recorded in 1376, little is heard of Popham before 1390, by which date, as he had become a knight, it seems likely that he had spent some considerable time engaged in military service abroad. In this, as in other respects, he differed from his elder brother, Henry, who, despite his wealth and standing, never took up knighthood. Like Sir Philip Popham, probably his uncle, who had served as bailiff of the duchy of Lancaster hundred of King’s Somborne since before June 1350 and received an annuity of £10 from the duchy until his death in 1397, Sir John found a patron in John of Gaunt.
Sir John was still alive in November 1417, when his brother Henry named him as an executor of his will, but he was not awarded administration of the Pophan estate on 22 June 1418, and died some time before 27 Oct. that year, when his son, Sir John junior, succeeded him as constable of Southampton castle. The Sir John who supervised musters there and served on commissions of array in April 1418 is most likely to have been the father, for the son had been appointed bailli of Caen the previous December and was certainly still in France in the early spring. The younger Sir John, who went on to lead a distinguished career as chamberlain to the duke of Bedford, chancellor of Anjou and Maine, and treasurer of the household of Henry VI, was elected Speaker in the Parliament of 1449 (Feb.), only to decline the office.